Literature DB >> 29537962

Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita.

Juan Jose Fraire-Zamora1,2, Johannes Jaeger2,3,4, Jérôme Solon1,2.   

Abstract

Evolution of morphogenesis is generally associated with changes in genetic regulation. Here, we report evidence indicating that dorsal closure, a conserved morphogenetic process in dipterans, evolved as the consequence of rearrangements in epithelial organization rather than signaling regulation. In Drosophila melanogaster, dorsal closure consists of a two-tissue system where the contraction of extraembryonic amnioserosa and a JNK/Dpp-dependent epidermal actomyosin cable result in microtubule-dependent seaming of the epidermis. We find that dorsal closure in Megaselia abdita, a three-tissue system comprising serosa, amnion and epidermis, differs in morphogenetic rearrangements despite conservation of JNK/Dpp signaling. In addition to an actomyosin cable, M. abdita dorsal closure is driven by the rupture and contraction of the serosa and the consecutive microtubule-dependent seaming of amnion and epidermis. Our study indicates that the evolutionary transition to a reduced system of dorsal closure involves simplification of the seaming process without changing the signaling pathways of closure progression.
© 2018, Fraire-Zamora et al.

Entities:  

Keywords:  Megaselia abdita; developmental biology; dorsal closure; evolution of development (evo-devo); evolutionary biology; extraembryonic tissue (serosa/amnion); genomics; microtubule cytoskeleton; stem cells; tissue seaming

Mesh:

Substances:

Year:  2018        PMID: 29537962      PMCID: PMC5851697          DOI: 10.7554/eLife.33807

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  45 in total

Review 1.  Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology.

Authors:  Antonio Jacinto; Sarah Woolner; Paul Martin
Journal:  Dev Cell       Date:  2002-07       Impact factor: 12.270

2.  Function of bicoid and hunchback homologs in the basal cyclorrhaphan fly Megaselia (Phoridae).

Authors:  M Stauber; H Taubert; U Schmidt-Ott
Journal:  Proc Natl Acad Sci U S A       Date:  2000-09-26       Impact factor: 11.205

3.  Sequential contraction and exchange of apical junctions drives zippering and neural tube closure in a simple chordate.

Authors:  Hidehiko Hashimoto; Francois B Robin; Kristin M Sherrard; Edwin M Munro
Journal:  Dev Cell       Date:  2015-01-26       Impact factor: 12.270

Review 4.  Morphogenetic functions of extraembryonic membranes in insects.

Authors:  Urs Schmidt-Ott; Chun Wai Kwan
Journal:  Curr Opin Insect Sci       Date:  2016-02-11       Impact factor: 5.186

Review 5.  Extraembryonic development in insects and the acrobatics of blastokinesis.

Authors:  Kristen A Panfilio
Journal:  Dev Biol       Date:  2007-11-17       Impact factor: 3.582

6.  Comparative transcriptomics of early dipteran development.

Authors:  Eva Jiménez-Guri; Jaime Huerta-Cepas; Luca Cozzuto; Karl R Wotton; Hui Kang; Heinz Himmelbauer; Guglielmo Roma; Toni Gabaldón; Johannes Jaeger
Journal:  BMC Genomics       Date:  2013-02-24       Impact factor: 3.969

7.  An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos.

Authors:  Bruno Monier; Anne Pélissier-Monier; Andrea H Brand; Bénédicte Sanson
Journal:  Nat Cell Biol       Date:  2009-12-06       Impact factor: 28.824

8.  High plasticity in epithelial morphogenesis during insect dorsal closure.

Authors:  Kristen A Panfilio; Georg Oberhofer; Siegfried Roth
Journal:  Biol Open       Date:  2013-09-05       Impact factor: 2.422

9.  Microtubule-dependent balanced cell contraction and luminal-matrix modification accelerate epithelial tube fusion.

Authors:  Kagayaki Kato; Bo Dong; Housei Wada; Miho Tanaka-Matakatsu; Yoshimasa Yagi; Shigeo Hayashi
Journal:  Nat Commun       Date:  2016-04-12       Impact factor: 14.919

10.  The beetle amnion and serosa functionally interact as apposed epithelia.

Authors:  Maarten Hilbrant; Thorsten Horn; Stefan Koelzer; Kristen A Panfilio
Journal:  Elife       Date:  2016-01-29       Impact factor: 8.140

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